observed and predicted effects of climate on australian seabirds

Observed and predicted effects of climate on Australianseabirds

Lynda E ChambersAG Carol A DevneyB Bradley C CongdonC Nic DunlopDEric J Woehler E and Peter DannF

ACentre for Australian Weather and Climate Research Bureau of Meteorology GPO Box 1289Melbourne VIC 3001 Australia

BAIMSJCU Marine and Tropical Biology James Cook University Cairns QLD 4870 AustraliaCMarine and Tropical Biology James Cook University Cairns QLD 4870 AustraliaDConservation Council (WA) 2 Delhi Street West Perth WA 6005 AustraliaESchool of Zoology University of Tasmania Sandy Bay TAS 7005 AustraliaFResearch Department Phillip Island Nature Parks PO Box 97 Cowes VIC 3922 AustraliaGCorresponding author Email lchambersbomgovau

Abstract Although there is growing evidence of climate warming for many regions the broader effects of climatevariation on marine top predators remains unknown owing to the difficulty in obtaining for synthesis long-term and short-term datasets on multiple species In the Australian region climatic and oceanographic variability and change have beenshown to affect marine species often with profound consequences Many seabirds are apex predators for which changes inclimatic and oceanic dynamics have driven range movements poleward reduced breeding success and altered breedingtiming for some species Here we review the literature to assess and determine the vulnerability of Australian seabirds tovariation and change in climate and identify which species and ecosystemsmay bemore resilient to future climate warmingIt is clear from this synthesis that not all Australian seabirds are affected similarly with responses varying by species andlocation In addition the paucity of information on the distribution and biology of seabird prey foraging patterns andmovements of seabirds and the ability of seabirds to switch between prey species or adjust timing of life-cycles makegeneralisations about potential effects of future climate change and adaptive capacity in seabirds difficult This applies bothwithin Australia and elsewhere where data are similarly sparse

Additional keywords climate change ENSO sea-surface temperature

Introduction

There is growing evidence that climate warming is adverselyaffecting marine ecosystems and species (Hughes 2000 Waltheret al 2002 Root et al 2003 Ainley et al 2010) Reproductiondistribution phenology and survival can all be affected by large-scale climatic processes such as the El NintildeondashSouthern Oscil-lation (ENSO) (Stenseth et al 2002 Mills et al 2008 Sydemanand Bograd 2009 Ainley andHyrenbach 2010) Climatic signalsfrom the marine environment at local scales (ie temperaturewind and precipitation) also affect demographic processes insome species (Aebischer et al 1990 Kitaysky and Golubova2000 Gjerdrum et al 2003) In some cases demography(eg reproduction and recruitment) can be influenced by bothlarge-scale and local processes (Sandvik et al 2005 Votier et al2005 Weimerskirch et al 2003) The effects of climatic vari-ability also differ among species owing to species-specific life-history characteristics foraging guilds and adaptation to localenvironments (Edwards and Richardson 2004 Post et al2009 Suryan et al 2009 Rolland et al 2010) Hence arange of complex dynamical environmental forces profoundly

influences which species and ecosystems are vulnerable topredicted future climatic changes (Tierno de Figueroa et al2010 Ainley and Hyrenbach 2010)

Many seabirds are apex marine predators that are heavilyinfluenced by variation in and changes to the marine environ-ment Such changes affect prey density and availability whichflow on to higher trophic levels with effects on abundancedistribution productivity behaviour and community structure ofseabirds (eg Ainley et al 1988 Velarde et al 2004 Richardsonet al 2006 Woehler et al 2006 Congdon et al 2007 Cullenet al 2009) This is particularly evident in regions where localsea-surface temperatures (SST) and marine productivity areinfluenced by upwelling dynamics and boundary currents(reviewed by Ballance et al 2006) For example higher SSTshave been linked to both reduced and improved breedingsuccess later breeding and increasedmortality in several seabirdspecies in the central and eastern Pacific Indian southernAtlantic and Southern Oceans (Ainley et al 1988 Crawfordand Jahncke 1999 Velarde et al 2004 Ramos et al 2006Woehler 2006) In contrast for surface-feeding birds in the

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north-western Atlantic Ocean reduced breeding success hasbeen associated with lower SSTs (Regehr and Montevecchi1997 Sandvik et al 2008)

Whether seabirds can respond to further predicted changes inenvironmental variability remains largely unknown (Greacutemilletand Charmantier 2010) Adjustments to characteristics such asbehaviour diet morphology geographical distribution or phe-nology to suit changing environmental conditions can fostergreater lifetime reproductive success (Nussey et al 2007 Reedet al 2009) and population viability Organisms with suchplasticity will generally be better able to cope with environmen-tal variation and extremes (Reacuteale et al 2003 Moe et al 2004Chiaradia and Nisbet 2006)

Most studies into the potential effects of current and futureclimate variability on seabird biology have focused on high-latitude species in the northern Pacific Ocean (Veit et al 1997Ainley and Divoky 2001 Bertram et al 2009) northern AtlanticOcean (Durant et al 2004 Sandvik and Erikstad 2008 Sandviket al 2008) and the Southern Ocean (Smith et al 1999 Croxallet al 2002 Jenouvrier et al 2003 Barbraud and Weimerskirch2006 Forcada and Trathan 2009) Considerably less is knownabout species living in the south-western Pacific or the waterssurrounding Australia (but see Mills et al 2008) As a conse-quence there is little broad-scale information about the degreeto which particular species populations or ecosystems arevulnerable to climatic variation and whether plasticity in life-history characteristics or adaptation is likely to moderate theseeffects

Australia and its external territories have a diverse seabirdfauna of 110 species in 12 families (van Tets and Fullagar 1984Ross et al 1995) Most (69) also breed in the Australianregion with the rest being either regular or occasional visitorsduring the non-breeding season (Ross et al 1995) Effectivelong-term conservation of this diverse fauna in the face ofpredicted climate change requires a detailed understanding ofthe influence of large-scale and local climatic phenomena onreproductive and other life-history parameters across a range ofseabirds including representatives from different foragingguilds

This review aims to collate and summarise information onthe relationships between population demographic and beha-vioural characteristics of Australian seabirds and key large-scaledrivers of climate in the Australasian region such as ENSO andassociated oceanographic changes sea-level rise land tempera-tures and extreme events including cyclones floods and fireThis information is then used to identify consistent long-term demographic trends potentially linked to specific climaticphenomenon establish the nature and likely magnitude ofeffects on different foraging guild and species assess theirpotential to cope with such effects and identify existing knowl-edge gaps

Observed and projected changes

Effect of changes in ENSO ocean temperaturecurrents and stratification

ENSO is a major contributor to Australiarsquos climate and affectsAustraliarsquos marine waters to differing degrees in different coastalregions ENSO has a strong and very significant effect on the

intensity of the southward flowing Leeuwin Current and watersof Australiarsquos western coast (Holbrook et al 2009) ENSO isobserved as a weaker signal in the southward flowing EastAustralian Current along Australiarsquos eastern coast El Nintildeoevents are associated with a range of climatic anomalies inAustralian waters including increased SSTs (Holbrook et al2009) SSTs in the waters surrounding Australia have warmedsignificantly since the early 20th century (+07C Lough 2009)and 6 of the 10 warmest years have occurred in the most recent10 years (based on data back to 1910) By the 2030s SSTsaround Australia are projected to be ~1C warmer (relative to1980ndash99) with slightly less warming to the south of thecontinent By the 2070s SSTs are projected to be between15ndash30C warmer with slightly less warming to the south ofthe continent and greatest warming east and north-east ofTasmania (Lough 2009)

At the Houtman Abrolhos Western Australia (Fig 1) in-creased breeding deferral and reduced success in Wedge-tailedShearwaters (Ardenna pacifica) and tropical pelagic-foragingterns (eg Sooty Tern Onychoprion fuscata) tends to occurduring stronger ENSO events (Dunlop et al 2002 Surman andNicholson 2009) probably owing to changes in marine produc-tivity driven by associated oceanographic changes (ie currentsSST) (Dunlop et al 2002) During El Nintildeo events the ternspecies also tended to breed later (Surman and Nicholson 2009)presumably as a result of ENSO-linked weakening of theLeeuwin Current and a zonal shift in productivity In contrasta combination of both large-scale and local climatic conditionsappears to influence the breeding dynamics of Wedge-tailedShearwaters in this region with the number of burrows exca-vated being related to the cumulative effect of oceanic conditions(eg Southern Oscillation Index (SOI)) from previous seasonsand the number of eggs laid being related to local weather andpredation (Dunlop et al 2002) Importantly these negativeeffects have only been observed for pelagic and offshore-for-aging species with no similar influences detected on the inshoreforaging Crested Terns (Thalasseus bergii) (Gaughan et al2002) This is mostly likely because they have more flexibleforaging behaviours (Surman and Wooller 1995 Blaber et al1998) Breeding success and breeding effort in Red-billedGulls (Chroicocephalus novaehollandiae scopulinus) inNew Zealand were strongly correlated with ENSO events andavailability of prey species (Mills et al 2008) The results for thisNew Zealand subspecies of the Silver Gull (C novaehollandiaenovaehollandiae) of Australia may provide insights intoclimatendashprey relationships for Silver Gulls and similar speciesin Australia

ENSO events have also been associated with WesternAustralian tropical seabirds (including Wedge-tailed Shear-waters Red-tailed Tropicbirds (Phaethon rubricauda) CrestedRoseate (Sterna dougallii) Sooty and Bridled Terns (Onycho-prion anaethetus) and Common Noddies (Anous stolidus))prospecting and nesting beyond their accepted breeding distri-butions on the western coast This suggests that in philopatricspecies ENSO-related marine productivity failures maydrive the dispersal of pre-breeders to foraging areas awayfrom natal colonies during the breeding season (Dunlop2009) If so then predicted background rises in sea temperature(Lough 2009) may then enable tropical seabird prey and seabird

236 Emu L E Chambers et al

frontier sub-colonies to persist at more southern latitudes(Dunlop 2009)

In the Great Barrier Reef (GBR) region (Fig 1) increasedSSTs have also been associated with reduced breeding successin seabirds mainly through reduced provisioning rates(Smithers et al 2003 Peck et al 2004 Congdon et al 2007)The available data indicate that there are SST limits abovewhich provisioning rates become so low that many pelagic andoffshore foraging species including the Sooty Tern BlackNoddy (Anous minutus) and Wedge-tailed Shearwater havezero or negative chick growth with concomitant low breedingsuccess (Congdon et al 2007)

Population trends of some species in the GBR region andCoral Sea have been negatively affected by suspected ENSOeffects (reviewed by Congdon et al 2007) Data from RaineIsland northern GBR indicate a potential progressivedecline in breeding populations of 10 of the 14 breeding species(Batianoff and Cornelius 2005) Although the cause is notknown changing climatic and oceanographic regimes or humaninfluences such as trawling or both are suggested as likelydrivers This is because there is no contemporary evidence ofsignificant human disturbance deterioration of nesting habitator habitat loss Populations of BrownBoobies (Sula leucogaster)have been declining at the Swain Reefs southern GBR inrecent years (Heatwole et al 1996 Congdon et al 2007)possibly as a result of decreases in food availability associatedwith significant El Nintildeo events Masked Boobies (S dactylatra)did not experience similar declines Populations of Great(Fregata minor) and Least Frigatebirds (F ariel) and possibly

Black Noddies in the Coral Sea also show declines (reviewedby Congdon et al 2007) again most likely as a result of effectsfrom significant El Nintildeo events Other species in the CoralSea (Red-footed Boobies (S sula) and Red-tailed Tropicbirds)have fluctuating populations whereas populations of somespecies have remained stable (Masked Booby and Wedge-tailedShearwater)

In temperate south-eastern Australia higher SSTs before thebreeding season of Little Penguins (Eudyptula minor) at PhillipIsland (Fig 1) are correlated with earlier laying and more andheavier chicks (Cullen et al 2009) However over the last40 years Little Penguins have been laying significantly later(~065 daysyear P= 0021) associated with a non-statisticallysignificant cooling of waters in northern Bass Strait duringMarch to May Higher SSTs have also been associated withincreased survival of first-year Little Penguins whereas thereverse appears to be true for adult survival (Sidhu 2007) Sootyand Bridled Terns as well as Lesser and Common Noddies havebeen laying significantly later since the 1980s at establishedcolonies off south-western Australia (Surman and Nicholson2009 J N Dunlop pers obs) This is coincident with a 013Cper decade rise in background sea temperatures in the region(Lough 2009)

Many seabirds can range thousands of kilometres on foragingtrips and may be able to shift their distributions rapidly inresponse to changes in the climatic system However suchflexibility is only possible if they are still able to access requiredcore habitat (ie nesting sites and feeding grounds) (Richardsonet al 2006) Some seabird species including many breeding at

10degS

20degS

30degS

40degS

10degS

20degS

30degS

40degS

110degE 120degE 130degE 140degE 150degE 160degE


Fig 1 Map of Australiarsquos major current systems and key seabird breeding locations

Observed and predicted climate effects on Australian seabirds Emu 237

Lord Howe Island (Fig 1) (DECC 2007) are already at theextremity of their breeding range and undertake long foragingtrips Therefore any southward shift in prey distribution asanticipated under warming oceans is likely to greatly affect thebreeding success and abundance of such species In WesternAustralia a farther southward shift in breeding distribution ofseveral tropical seabirds is expected together with decreases inpopulation sizes on the Houtman Abrolhos (Dunlop 2009)Frontier colonies south of the former breeding range maycontinue to appear and establish but the overall size of theregional metapopulations is likely to be well below historicallevels owing to the distances between breeding islands andpotentially productive foraging regions (eg the continentalshelf-edge) (Dunlop 2009)

Projected changes in ocean temperatures and ENSO-typeactivity may reduce prey availability during the breeding seasonresulting in increased deferred breeding and reduced success(reviewed by Congdon et al 2007 Table 1) In addition ifseabird prey undergo rapid shifts in distribution either verticallyor horizontally in order to remain in preferred water tempera-tures they may become less accessible to seabirds on a day-to-day basis particularly if the abundance of subsurface predators(eg tuna Thunnus spp) which herd prey towards the surfacealso decreases (Peck et al 2004 Erwin and Congdon 2007Devney et al 2010)

Regression models for tropical pelagic species demonstratezero (or negative) chick growth for SST increases of 24Cabove current averages (Congdon et al 2007) Howeverthe extent of chick starvation and colony-wide reproductivefailure also depends on the length of time that the SST remainsabove current ranges the stage of chick development and thespecies involved (Congdon et al 2007) In contrast there isevidence that at least some southern species may benefit fromincreasing SSTs at least in the immediate future including theLittle Penguin which may breed earlier and more successfullyin years of higher SSTs (Cullen et al 2009)

Alterations to currents mixed-layer depths and oceanstratification also have the potential to affect seabird distribu-tions migration and foraging via their effects on nutrientsand light and consequently prey species and subsurface pre-dators (Ballance et al 2006 Poloczanska et al 2007) Changesin these physical properties can also alter processes thatconcentrate prey species such as fronts and eddies thatare used by seabirds as foraging cues (Hunt and Schneider1987 Hyrenbach et al 2006 2007 Woehler et al 2006 Nevitt2008)

In the Australian region the East Australia Current theAntarctic Convergence and the Leeuwin Current (Fig 1) strong-ly influence marine productivity and seabird distributions (Bla-ber et al 1996) Although there is significant spatial andtemporal variability the surface waters of the East AustraliaCurrent are typically low in nutrients (Roughan and Middleton2002) Data from the GBR suggests that nutrient hotspots areimportant to seabirds and these are few in number and locatedadjacent to Coral Sea mounts and along the eastern edge of thecontinental shelf (Congdon et al 2007) Seabird breeding suc-cess in the GBR may be dependent on the persistence of a lownumber of these highly productive areas (Congdon et al 2007)

Short-tailed Shearwaters (Ardenna tenuirostris) breedingin south-eastern Australia strongly associate with physical oce-anic features on their foraging trips to the Southern Ocean(Woehler et al 2006 Raymond et al 2010) These featuresconcentrate prey in spatially or temporally predictable areas andthe Shearwaters use wind fields between their colonies andforaging locations (Raymond et al 2010) Periods of peakreliance on the Antarctic Polar Front and the Antarctic Diver-gence vary with altering energy costs associated with breeding(Woehler et al 2006 Raymond et al 2010) Rising air and oceantemperatures may result in changes to the wind regime over theSouthern Ocean and to the onset or rate of the seasonal ice-meltthat triggers enhanced productivity close to the Antarctic con-tinent where the shearwaters forage and may influence theenergy budgets of foraging shearwaters (Greacutemillet and Boulinier2009)

In association with predicted future global warming the EastAustralia Current is projected to transport warmer water farthersouth The Leeuwin Current is expected to be similarly affectedby lsquosuperrsquo La Nintildeas such as that during 1999ndash2001 (Holbrooket al 2009) This implies that both current systems will carrysubtropical prey species into temperate waters well south oftheir previous distributions and substantially alter the habitat ofmany species (Dunlop 2009 Surman and Nicholson 2009) Forseabirds competition with established species for nesting sitesand foraging habitat is likely to result from these new invasions(Dunlop 2009) Changes in oceanic stratification measured byvariation in the depths of warm and cold water masses are wellknown precursors to ENSO events (eg McPhaden and Yu1999) Changing distributions and catastrophic breedingfailure in both temperate and cold-tropical seabird breedingpopulations have been linked to El Nintildeo events (Schreiber andSchreiber 1984 Oedekoven et al 2001 Bertram et al 2005)through their effects on nutrient upwelling or mixing In warmtropical regions such as the GBR and adjacent Coral Sea whereupwelling is aseasonal and nutrient-rich waters are localised(Andrews and Gentien 1982) the influence of thermoclinevariability is not well known At Michaelmas Cay northernGBR individual seabird species appear to be affected differentlyby changes in key oceanic characteristics depending on theirforaging guild Deferred breeding in pelagic-foraging tern spe-cies (Sooty Terns and Common Noddies) but not inshore-foraging species (Crested Terns) (Devney et al 2009a) wasdriven by surface chlorophyll concentration and depth of the20C thermocline in the year preceding a formal El Nintildeo eventReduction in thermal stratification of coastal water masses hasalso been linked to foraging and breeding success in the tem-perate Little Penguin (Phillip Island) (Ropert-Coudert et al2009) with prey thought to disperse widely in poorly stratifiedwaters

It is currently unclear what effect any future changes inmixed-layer depth and oceanic stratification will have onproductivity prey aggregation and prey availability to foragingseabirds This is particularly true in the Coral Sea region wheredepth of the 20C thermocline can exceed 200m (Devney et al2009a) (compared with depths of 20ndash40m in the eastern tropicalPacific Ocean Ballance et al 2006) and most tropical pelagicseabirds are wholly reliant on subsurface predators such as tuna


Table 1 Summary of observed and projected climate-related changes in Australian seabirdsAdapted from Chambers et al (2009b) GBR Great Barrier Reef

Observed change Amount of evidence or confidence in assessment Projected future changes

OceanTropical and subtropical

species decreases related toENSO-associated increasein SSTs

LowndashMedium Likely continued decreasing trends includingdecrease in seabird populations of the HoutmanAbrolhos

Raine Island GBR population decreases in 13 of 16species over 24-years period ndash no evidence ofhuman disturbance or reduction in habitat quality ndashprobably related to ENSO-associated SST increasebut no direct data linking variables (Batianoff andCornelius 2005)

Swain Reefs GBR population decreases in BrownBooby and Silver Gull Reductions in foodavailability probably associated with ENSO-associated increases in SST but no direct datalinking variables (Heatwole et al 1996)

South-western Australia poor reproductiveperformance of 7 species during El Nintildeo periods inlast 3ndash4 decades (Dunlop 2009)

Corroborating studies outside Australia (eg Ramoset al 2002)

Population increase insubantarctic seabirdsassociated with regionalwarming (ocean and air)

MediumHeard Island populations of King Penguins

(Aptenodytes patagonicus) and Black-browedAlbatross (Thalassarche melanophris) increased

Penguin populations likely to increase until availablebreeding habitat is exhausted Competition withincreasing fur seal (Arctocephalus spp) populationalso likely to limit population growth

Albatross population on Heard Island likely toincrease as glacier recession provides additionalbreeding habitat

since 1947 as glaciers retreat to provide additionalhabitat (Woehler 2006 Woehler et al 2002)

LowndashMediumMacquarie Island population of King Penguins

increasing as air temperatures increase regionally(Pendlebury and Barnes-Keoghan 2007 Trathanet al 2007) Regional trend at Macquarie Islandreflects global increase in species

Southward shift in breedingdistributions of tropicalspecies associated with risein regional SST

Medium Shift in breeding distribution southwardsSouth-western Australia rapid growth of colonies of

7 species in last 3ndash4 decades at southerndistributional limits and frontier colonies south ofhistorical breeding range (Dunlop 2009)

Reduced foraging success andchick growth in tropical andsubtropical seabirdsassociated with increasedSSTs

Low Reduced breeding success owing to decreasedseasonal prey availabilityWedge-tailed Shearwater Heron Island GBR

increased SSTs associated with seasonal-scaledecreases in prey availability possibly owing todecreased productivity at lower trophic levels(Smithers et al 2003 Peck et al 2004)

Sooty Tern Michaelmas Cay GBR and BlackNoddy Heron Island GBR increases in SST causeforage fish or subsurface predators or both tomove either horizontally or vertically decreasinginteractions with foraging seabirds (Erwin andCongdon 2007 Devney et al 2010)

Decreased prey availability or greater potential fortemporal and spatial reductions in prey availabilityto coincide with important reproductive stages

Corroborating studies outside Australia (Gjerdrumet al 2003 Quillfeldt et al 2007)

Reduced chick survivalassociated with increasedSSTs (subtropical)

Low Reduced breeding success due to decreased seasonalprey availabilityWedge-tailed Shearwater Heron Island GBR


(Continued next page)


Table 1 (continued )


Delayed breeding associatedwith shift in peak SSTs

LowndashMedium UnknownSouth-western Australia significant delay in timing

of laying post-2000 in Bridled Tern (PenguinIsland) and Sooty Tern Common Noddy andLesser Noddy (Pelsaert Island HoutmanAbrolhos) Decrease in spring productivitythroughout the region Shift in the peak in SSTsinto late autumn (Surman and Nicholson 2009J N Dunlop unpubl data) Confident that ENSOis a driver of change but the new factors (post-2000)causing a retreat in breeding dates and failures innon-El Nintildeo years are complicating theinterpretation

Timing and success ofbreeding temperate speciesrelated to SSTs

LowndashMedium Models predict a reversal of trend towards laterbreeding and suggest improved growth of thecolony at least in the immediate future

Phillip Island Victoria breeding in Little Penguinsover the last 40 years has become later timing ofbreeding number of chicks produced per pair andchick mass at fledging related to Bass Strait SSTs ndashpresumed to have significant influence on foodavailability (Cullen et al 2009) Foraging areascorrelated with narrow band of SSTs during chick-rearing (Hoskins et al 2008) For Little Penguinsbreeding in eastern Australia there is an inverserelationship between the latitude of the breedingcolony and breeding success perhaps the result ofthe reduced positive effects of the East AustralianCurrent at higher latitudes (Fortescue 1998)

Medium UnknownIn New Zealand breeding effort (proportion of

population breeding) and breeding success (chicksfledged) mean egg-masses and mean laying datesof Red-billed Gulls are influenced by SOI whichinfluences prey species (zooplankton) availabilityduring breeding season Red-billed Gulls aresubspecies of Silver Gulls of Australia which alsotake the same zooplankton prey speciesNyctiphanes australis (OrsquoBrien 1988)

Temperate species survivallinked to SSTs (relationshipdiffers between juvenile andadult birds)

LowndashMedium UnknownPhillip Island Victoria based on 22 years data

increased survival of first-year Little Penguinsassociated with higher SSTs the reverse for adultsurvival (Sidhu 2007)

Restricted capacity to adjustlife-history characteristics

Low No mediation of climate effects on reproductivesuccess via developmental or behavioural plasticityHeron Island GBR Black Noddy has restricted

capacity to adjust life-history characteristics tocompensate for changes in prey availabilityassociated with rapid environmental change(Devney et al 2010)

Breeding participation intropical pelagic species butnot inshore species relatedto ENSO-associatedchanges in thermoclinedepth and levels ofchlorophyll-a

LowndashMedium Projected increases in either the frequency or intensityof El Nintildeo precursors is likely to result in increaseddeferred breeding with flow on effects torecruitment

Michaelmas Cay GBR for 3 species decreases inboth marine productivity and thermocline depth upto 12 months preceding a registered ENSO eventinfluenced breeding participation in pelagicforaging species only (Devney et al 2009a)

Reduction in thermoclinelinked to decreased foragingand breeding success(temperate seabirds)

LowPhillip Island Victoria reduction in thermocline

associated with decrease in foraging and breedingsuccess in Little Penguins (Ropert-Coudert et al2009) Local-scale ocean temperature dominantfactor in breeding success indices of ENSO linkedto hatching success (Chambers 2004)


and marine mammals to drive prey to the surface (Au and Pitman1986 Jaquemet et al 2004) However changes in the frequencyor intensity of ENSO and associated precursors (including

changes to ocean stratification) are likely to affect pelagicseabird breeding participation and population dynamics in thenorthern GBR



Population decreases in Red-tailed Tropicbird may berelated to variation inLeeuwin Current

LowSouth-western Australia population decrease in Red-

tailed Tropicbird was unexpected and may berelated to variations in Leeuwin Current (Garnettand Crowley 2000)

Wind storms and cyclonesShort-term effects from

individual cyclones aremediated in the long term

Low Increased occurrence of extreme storms has thepotential to overlap spatially and temporally withimportant reproductive stages Increased chance ofhypothermia among chicks who are exposed to thewind

Michaelmas Cay GBR for 3 species increased eggand chick mortality owing to inundation decreasedprey availability influences subsequent recruitmentor breeding success or both (Devney et al 2009b)

Cyclones and strong windsaffect breeding participationand timing

LowndashMediumMichaelmas Cay GBR cyclones and strong winds

alter the periodicity of Sooty Tern breeding andaffect breeding numbers and success of both SootyTern and Common Noddy as nests can be lostthrough wave inundation and erosion and eggs andchicks lost from exposure starvation and adultdesertion (King et al 1992)

Strong winds and cyclonesincrease adult mortalityreduce fledging andbreeding success

Low Higher SSTs could result in lower breeding successfor Abbottrsquos Booby regardless of nest location Asmost Christmas Island Frigatebird (Fregataandrewsi) nests are located in a single colony thespecies is particularly vulnerable to cyclones orforest fires Higher SSTs may also reduce foodavailability in nearby marine areas

Christmas Island in wind-affected areas increasedturbulence caused higher adult mortality andreduced fledging success of Abbottrsquos BoobySevere storms have marked effect on reproductiverate in ensuring years Abbottrsquos Booby probablyrelies on seasonal increase in fish numbersassociated with cold-water upwellings to raise theiryoung ndash SST data strongly correlated with annualbreeding success (Reville et al 1990 Garnett andCrowley 2000 DEH 2004)

Christmas Island many Christmas Island Frigatebirdeggs can be lost during a single breeding season dueto strong winds and cyclones (Garnett and Crowley2000) In the Lesser Noddy nest sites protectedfrom strong WNW winds are more likely tosucceed than exposed nests (Garnett and Crowley2000 Hill and Dunn 2004)

Stronger winds beforebreeding season related tolater start to breeding

LowPhillip Island Victoria strong westerly winds in

JanuaryndashMarch correspond to later breeding inLittle Penguins Westerly winds may accelerate theenriched prevailing water currents from the westtowards feeding grounds (Chambers 2004)

Other extreme events (including fire)Hot dry weather associated

with increased risk ofpower-pole firessynchronised burrowingspecies vulnerable

Low Increase in hot dry weather in southern Australia mayincrease fire-related risk of seabird death andinjury Risk compounded by increasing coastaldevelopment

Phillip Island Victoria number of fires in recent yearsfrom build-up of salt and dust on power-poleinsulators following long hot dry spells LittlePenguins do not avoid fire birds nesting undervegetation remain until severely burnt or killedSynchronised breeding of seabirds increasesvulnerability to fires during nesting seasonsparticularly for burrow-nesting species that aredisinclined to abandon nests or emerge in daylight(Chambers et al 2009a 2009b)


Effect of rises in sea level

There are no known quantitative links between observed sea-level rise and changes in the distribution and abundance ofnesting Australian seabirds The effect of future rises in sealevel on seabirds is expected to vary with breeding habitat withhigh rocky islands less at risk than low-lying and less stableislands (Sharples 2006 Bennett et al 2007) Many species ofbirds are dependent on coastal habitats for nesting feeding androosting These habitats are at risk from rises in sea level Birdspecies affected may include many species of migratory shore-birds species that nest or forage in mangroves and species thatbreed on low-lying sand cays or on sandy beaches (Richardsonet al 2006 Bennett et al 2007) The potential for shorelines toevolve naturally in response to rises in sea level may be con-strained by coastal development and infrastructure (Richardsonet al 2006 House of Representatives 2009) This will alsoconstrain the ability of seabirds to alter their nesting locationsand inshore foraging habitat and may lead to an increase inseabirds breeding on artificial structures (eg Erwin 1980Coulson and Coulson 2008)

Seabirds breeding in low-lying parts of islands are atrisk of inundation Such risks occur on islands of the TorresStrait Houtman Abrolhos GBR and in the Lord HoweIsland group (Ross et al 1996 Garnett and Crowley 2000Congdon et al 2007 DECC 2007 Table 1) Increased inter-specific competition as a result of sea-level rise may occur insome regions for example increased sand deposition mayallow turtles to access the central depression of Raine Island(GBR) currently used by ground-nesting seabirds (Congdonet al 2007)

Effect of changes in land temperature

Higher land temperatures can increase heat stress and mortalityleading to reduced breeding success particularly for surface-dwelling birds such as penguins (Stahel and Gales 1987 Cullenet al 2009)Many seabirds including Little Penguins are unableto withstand prolonged exposure to air temperatures above35C (Stahel and Gales 1987) Even a few hours of burrowtemperatures above this can lead to dangerously high bodytemperatures in Little Penguins (Stahel and Gales 1987) heatstress accounts for ~02 of annual adult mortality (Dann1991) It has been suggested that winter breeding in Pied(Phalacrocorax varius) and Black-faced (Ph fuscescens)Cormorants in south-eastern Australia which is unlike themajority of seabirds in this region (Norman 1974 Taylor2007) is to avoid heat stress in young and adults (Taylor2007) Long-term increases in land temperatures along withdrought periods have also indirectly affected seabirds on theGBR by contributing to dieback of stands of Pisonia grandis(Batianoff et al 2010) which is crucial nesting habitat for BlackNoddies andWedge-tailed Shearwaters (Walker 1991 Batianoffet al 2010)

The potential future effects of increased air temperaturesinclude the obvious potential detrimental effect of heat stress(Stahel and Gales 1987 Dann 1991 Taylor 2007) as well as amyriad of potential bottom-up effects to seabird prosperity(reviewed by Greacutemillet and Boulinier 2009) such as drivingwarming of surface waters sea-level rise reductions in vertical

mixing of oceanic waters melting of Arctic and Antarctic icestronger winds and more frequent storms and cyclones

Effect of ocean acidification

There are no known quantitative links between ocean acidifica-tion and changes in the distribution and abundance of nestingseabirds and it is currently uncertain what effects future changesin oceanic chemistry will have on seabirds In tropical regionsocean acidification is expected to compromise coral reefaccretion through effects on the ability of corals to calcify andgrow (Hoegh-Guldberg et al 2007) thereby altering thecomposition of coral reef communities This could degradeimportant foraging habitat for nearshore feeding tropical sea-birds and breeding habitat for all taxa breeding in coral reefsystems such as the GBR Ningaloo Reef (Fig 1) and theHoutman Abrolhos

Pelagic marine organisms in both temperate and tropicalsystems are also not immune to the threat of ocean acidification(Doney et al 2009 Smith 2009) Decreases in marine biodi-versity are likely as organisms that produce a calcium carbonateskeleton such as plankton are reduced as a food source acrossthe trophic scale (Cicerone et al 2004 Dupont et al 2010)Similarly the availability of shelter and nursery areas for othermarine animals such as forage fish is also threatened (Smith2009) However overall effects remain unclear with futurechanges in seawater pH combined with projected temperatureincreases likely to favour some species of phytoplankton andzooplankton (Orr et al 2005)

Wind storms and cyclones

Changes in storm intensity strong winds and cyclones can affectforaging and nesting habitats and so significantly alter seabirdbreeding success (Table 1 and references therein) Cyclones cancause catastrophic destruction of breeding colonies and highmortality in tropical and subtropical Australia Cyclones can alsohave indirect effects through wave inundation during stormsurges erosion under the influence of gale-force winds stormtides and intensified currents (Blomqvist and Peterz 1984Congdon et al 2007 Devney et al 2009b) Sand cays whichare highly dynamic systems at the mercy of coastal processessuch as erosion and accretion are particularly vulnerable tostorms erosion of one part of the cay often being matched bysand deposition in another location (King 1996) In addition toon-island effects storms and cyclones can also negatively affectseabirds at-sea (Weimerskirch et al 2005 Richardson et al2006 Congdon et al 2007) Secondary effects of adverseweather during storms and cyclones also kills birds directlythat is via chilling that leads to hypothermia or indirectly bystarvation because adults are unable to forage effectively For-aging is affected by water turbidity associated with strong windsor sea-surface conditions that reduce visual acuity (Eriksson1985 Henkel 2006)

Cyclonic activity during critical nesting stages significantlyaffects breeding in some tropical seabirds (Langham andHulsman 1986 Congdon et al 2007 Devney et al 2009b)This in-turn influences the timing of breeding as well as short-term breeding participation and success (King et al 1992Devney et al 2009b) However short-term negative effects


from localised direct disturbance do not appear to have translatedinto long-term population decreases for species breeding in thenorthern GBR (Sooty Tern Common Noddy and Crested TernDevney et al 2009b) presumably because recovery periodsbetween events have been sufficient (Devney et al 2009b)However any future increase in the frequency or intensity ofstorms and cyclones increases both the spatial and temporalprobability that they will overlap sensitive breeding stagesreducing the recovery time or potential for successful breedingbetween events or both (Congdon et al 2007 Table 1)

Non-cyclonic storms and strong winds can also influencebreeding phenology (Chambers 2004) and breeding successby reducing foraging success increasing mortality of juvenilesand by flooding nests or nesting burrows (eg Roseate TernsBlaber et al 1996 Black Noddy Hulsman 1977) In southernAustralia storm and tidal damage to burrows can locally influ-ence numbers of seabirds such as Little Penguins at TroubridgeIsland South Australia (Fig 1) (Ross et al 1996) Storms canalso exacerbate food shortages or reduce the ability to obtainprey with mass mortality of seabirds along the Victorian coastoften following periods of strong winds (Norman et al 1996Ropert-Coudert et al 2009)

Storms are less likely to pose a major risk to populationsthat are large and spread over broad geographical areas (Garnettand Crowley 2000) However species or subspecies thathave small populations and restricted breeding distributionsare susceptible to catastrophic wind and storm events includingthe Australian populations of the temperate Fairy Prion(Pachyptila turtur) Blue Petrel (Halobaena caerulea)Gouldrsquos Petrel (Pterodroma leucoptera) White-necked Petrel(Pt cervicalis) Soft-plumaged Petrel (Pt mollis) Herald Petrel(Pt heraldica) Trindade Petrel (Pt arminjoniana) KermadecPetrel (Pt neglecta) and Grey-backed Storm-Petrel (Garrodianereis) (Garnett and Crowley 2000)

Precipitation floods terrestrial runoff and otherextreme events

There are few known direct effects of rainfall on survival orbreeding success of seabirds other than occasional heavy rainfallflooding seabird burrows (P Dann B Congdon pers obs) andchick mortality from hypothermia related to rainfall in combi-nation with wind chill (Langham and Hulsman 1986) Howeverrainfall may indirectly affect seabirds through its affect onavailability of prey quality of breeding habitat and fire risk todrying vegetation Anchovies (Engraulis australis) an impor-tant prey of Little Penguins (Chiaradia et al 2003) use estuarineregions when spawning and their productivity may be reducedwith decreasing stream flows into coastal areas (Santojanni et al2006) Estuaries may provide a nutrient and carbon subsidy tocoastal environments dependent on rainfall and flushing (Jacobset al 2002 Greene and Pershing 2007) and interannual varia-tions in estuary flows may affect breeding performance in LittlePenguins in the southern metropolitan coastal waters of Perth(J N Dunlop pers obs)

There are no known quantitative links between observedlong-term changes in rainfall and changes in the distributionand abundance of nesting seabirds in the Australian regionHowever increased duration of droughts and increased tem-

peratures (see lsquoEffect of changes in land temperaturersquo sectionabove) associated with climatic variation are thought to becontributing factors to the dieback of vital breeding habitat onthe GBR (Batianoff et al 2010)

Although it is uncertain what effect future changes to pre-cipitation floods and runoff will have on Australian seabirdsaltered rainfall patterns combined with rises in sea level mayinfluence seabirds and their reproductive success through theireffect on availability of breeding habitat (reviewed by Congdonet al 2007) The long-term effect is expected to vary according totheir relative affects on the distribution and abundance ofspecies-specific habitat (Turner and Batianoff 2007) In tropicaland subtropical regions reduced rainfall and increased sand andrubble deposition on windward island edges favours colonisingground covers and woody shrubs (Turner and Batianoff 2007)This may negatively affect species that nest in trees andburrows However the full extent of the effect will depend onhow limited by habitat availability the seabird colonies arecurrently (Congdon et al 2007)

Flow regimes and discharge patterns for major coastal rivershave the potential to affect seabirds through their effects onprimary productivity and trophic stability at lower trophic levelsand via nutrient enrichment of coastal waters (Grimes 2001Santojanni et al 2006)

Fire risk is increased during prolonged periods of hot dryconditions including fires resulting from built up salt and dust onpower-pole insulators such has occurred in recent years onPhillip Island Victoria a major Little Penguin breeding colony(Chambers et al 2009a) As breeding in many seabirds issynchronised the vulnerability of colonies to catastrophicevents such as fire during nesting seasons is increased Bur-row-nesting species such as Little Penguins shearwaters andpetrels are particularly vulnerable as they are reluctant toabandon nests or emerge during daylight Some seabird speciesincluding Little Penguins do not avoid fire and will remainunder or near vegetation until severely burnt or killed (Chamberset al 2009a) Any increase in the incidence or frequency ofhot and dry conditions is likely to increase fire related risk ofseabird injury and death particularly for burrowing colonialseabirds such as penguins (Chambers et al 2009a)

Assisting seabirds to adapt to climate change

Species may be able to cope with climate variation and futureclimate change by adjusting life-history characteristics such astiming of breeding foraging behaviour size of offspring growthrates of offspring or breeding location (Reed et al 2009)However plasticity of responses or adaptation potential ofseabirds is not well known both globally (Greacutemillet and Char-mantier 2010) and in Australia (Table 1) When Black Noddiesbreeding on the southern GBR faced wide variation in SST andassociated changes to prey availability adults were unable tomodify their foraging behaviour (prey type feeding frequency ormeal size) and chicks did not demonstrate variable growthrates (Devney et al 2010) These limitations suggest that theability of this species to buffer climate change by alteringbehaviour or via developmental plasticity is limited and adap-tive responses are therefore more likely to arise via naturalselection (Devney et al 2010) Provisioning adult Little


Penguins in south-eastern Australia experienced similarinability to adjust their foraging behaviour during periods ofdecreased food availability presumably owing to their shortforaging ranges (Chiaradia and Nisbet 2006) Little Penguinchicks responded to reduced provisioning rates by reducingmassgrowth (lsquoimposedrsquo response) and by delaying development(lsquoinducedrsquo response) (Chiaradia and Nisbet 2006)

Some climate effects on seabirds vary between locations(Table 1) which makes it difficult to generalise about adaptivecapacity This suggests that regional or colony-by-colony assess-ments of resilience or adaptive capacity may be required (Con-gdon et al 2007) However there are some general principlesthat could aid adaptations of populations to climate changeacross a range of species and regions (Olsen 2007)

Compensatory measures

Buffering potential negative effects of climate changethrough habitat management

In the short term there is some potential to buffer the expectednegative effects of climate change bymanaging terrestrial habitatquality and quantity For example at many temperate seabirdbreeding locations the vegetation has been severely modified bygrazing introduced plants and fire regimes (Norman 1970Weerheim et al 2003 Dann and Norman 2006) Several seabirddemographic parameters appear to be sensitive to the floristicsand structure of vegetation and associated microclimates Activemanagement of these can provide optimal microclimates forbreeding success and adult survival potentially mitigating somenegative effects of climate change (Dann and Chambers 2009)Some examples include

Reducing the potential for erosion by waves storms orrainfall by protecting or increasing appropriate vegetation andreducing inappropriate vegetation (Dann and Chambers2009)

Shading nests (either through natural vegetation or artificialstructures (as has been done for terns Voigts 1999) ordesigning insulated artificial nesting burrows to reduce heatstress in nesting seabirds (Dann and Chambers 2009)

Running powerlines underground and implementing a fast-response fire action plan to reduce the risk of fire in seabirdcolonies close to human settlements (Chambers et al 2009a)

Increasing the resilience of seabirds to the negativeeffects of climate change

Non-climatic pressures adversely affect many seabird popu-lations including pollution (Votier et al 2005) commercialfisheries (Frederiksen et al 2004 Lewison et al 2004) tourism(Rodgers and Smith 1995 Carney and Sydeman 1999) and feraland invasive animals and plants (reviewed by Fischer and vander Wal 2007 Clout and Russell 2008) Reducing or eliminatingthese threats will improve both the likelihood of successful(autonomous) adaptation and viability of populations thusreducing the overall risk of ecosystem collapse (Chamberset al 2005 Steffen et al 2009) Both land and sea componentsof the life-histories of species and associated threats need to beconsidered holistically rather than in isolation

Although options for the manipulation or management ofmarine habitats seem far less achievable than those in theterrestrial domain increasing resilience to climatic effectsmay be achieved by reducing other negative anthropogenicinfluences on foraging efficiency or threats to individualswhile foraging Appropriate actions may include a more pre-cautionary approach to the management of pelagic fisheriestargeting forage-fishes bill-fish tuna mackerel squid and krilland others mitigation of lethal effects of long-line fishing onseabirds no-take areas where fishing is prohibited and marineprotected areas to enhance recruitment of prey stocks andmaintain subsurface predator levels (Devney and Congdon2009)

Land-based actions include control or eradication of intro-duced feral and pest animals and plants such as Red Foxes(Vulpes vulpes) and Dogs (Canis lupus familiaris) and protec-tion of nests including cages or exclusion zones to reducepredation by introduced species and public interference withbreeding areas (eg Devney and Congdon 2009 Steffen et al2009) Further research is required to determine which regionsand species would most benefit by reductions in non-climatechange pressures (Chambers et al 2005)

Ex situ conservation or translocation

Ex situ conservation and translocation of species have tradi-tionally been considered a lsquolast resortrsquo for species that are unableto self-adapt However such intensive management optionsmay become increasingly important as more species face thethreat of extinction in the wild (Steffen et al 2009) Bothmeasures raise ethical issues such as lsquowhat effect will translo-cated species have on existing species in the recipient areasrsquo

Autonomous adaptation

At least in the short term the adaptive capacity of seabirds torespond to SST-associated changes in prey availability willdepend on the ability of a species to alter their foraging behaviour(including foraging location and prey species) nesting locationtiming of breeding or chick growth In some species such asWedge-tailed Shearwaters breeding in the southern GBR adultsalternate multiple short foraging trips to near-colony but re-source-poor areas with longer trips to more highly productivebut distant areas (Congdon et al 2005 Peck and Congdon2005) This strategy enables birds to breed in areas that wouldotherwise not support stable breeding populations (Congdonet al 2005) This implies that for some pelagic seabirds theirability to increase foraging rates may be extremely limited andthat if productivity remains low for several years relative tothe age at first breeding then there is a risk that colonies maybecome unviable (Congdon et al 2007) Some seabirds may beable to adapt to changes in the frequency and intensity ofcyclones and storms by adjusting either breeding timing toavoid periods of peak storm activity or relocating to less affectedbreeding sites The capacity for Australian seabirds to do eitherof these in response to these climate drivers is largely unknownand warrants further study (Congdon et al 2007)

The capacity of seabirds to adapt to rises in sea level andsignificant changes in rainfall depends on their ability to relocateto suitable alternative breeding sites (Congdon et al 2007)


assuming these habitats exist For those species that readily useartificial habitats such as navigation structures breakwaters orartificial islands some capacity exists for providing breedinghabitat above rising sea levels However apart from MacquarieIsland (and associated other subantarctic islands of NewZealand) there is little scope for seabird species of southernAustralian to shift southwards owing to the absence of landmasses south of Tasmania The existence of these alternativeswill depend on a complex mixture of factors including effects -associated with climate change on ocean acidification and coralgrowth precipitation shifts in key foraging locations and inter-actions with other processes including human disturbanceinfrastructure and competition with conspecifics

Research priorities

For many seabirds and regions only limited informationis presently available on prey distributions and biologyforaging and movement patterns and the ability of seabirds toalter prey species or life-cycle timing (Greacutemillet and Boulinier2009) All of these factors prevent the formulation of general-isations about potential effects of future climate change andadaptive capacity in seabirds and highlight the need for animproved knowledge base Based on this review (see alsoTable 1) there are several critical knowledge gaps requiringresearch investment

Although this review highlights advances made inrecent years we are only just beginning to understand theprincipal drivers of change in seabird populations includingthe relative role of natural variability and climate change com-pared with anthropogenic influences This needs to be investi-gated at the level of species ecosystems and bioregions andincludes an understanding of which processes and phases of lifecycles are most likely to be affected

Closely linked to this is a better understanding of what factorsdetermine the resilience and adaptive capacities of marineecosystems including seabirds In particular it is important tounderstand (1) which species and systems are most vulnerable(2) what levels of change species can tolerate while remainingviable (3) the relative effect of gradual events (eg sea-level risemean temperature) versus extreme events (eg cyclone andstorm surge frequencies) (4) potential climate thresholds ortipping points for species (5) how existing non-climatic threatsto seabirds interact with climate change (ie how to deal withcumulative effects) and (6) how to best utilise effort andfinancial resources and strategies to increase resilience by char-acterising interactions and synergies among stressors

Limited knowledge of some ecosystems species and bior-egions prohibits detailed analyses and predictions Researchis required to determine at what level and for what ecosystemsspecies and bioregions can appropriate generalisations be madeabout climate change effects and adaptation options includingdetermining appropriate temporal and spatial scales and poten-tially identifying indicator species of ecosystem health

At present we have only a limited knowledge on the dis-tributions and feeding movements of many seabird speciesparticularly outside the breeding season and of predation andcompetitive interactions (Brown et al 2010) This includes alack of information on primary foraging areas dispersal migra-

tion and inter-colony movements of seabirds and on species-specific diets including the trophic level or levels of prey preydistribution and the responses to climate change of prey andpredator species

Consideration also needs to be given to incorporating uncer-tainties in changes in the distribution of species changes inspecies interactions and ecosystem responses into currentmodelling of climate change effects on seabirds (Brown et al2010) The models need to be capable of modelling bioregionalchanges at spatial and temporal scales appropriate for manage-ment programs and reserve design (Brown et al 2010) Manyseabirds are long-lived and have low annual breeding-efforts(ie k-selected Begon et al 1996) with some species of seabirdstypically foraging widely during the breeding season (in somecases at spatial scales of ocean basins or greater) The predictivemodels must incorporate these aspects of the biology of speciesin order for the models to be relevant and applicable to theseabird species under consideration

Conclusions

For seabirds in the Australian region changes in climatic andoceanographic processes have been associated with changes inbreeding distributions breeding success breeding phenologychick growth and adult survival over many foraging guildsMost of the evidence for this region indicates that species arebeing negatively affected by climatic variability associated withEl Nintildeo events increased SSTs and incidences of extremeweather (ie tropical cyclones major storms and heat events)Documented effects for Australian waters also include speciesprospecting farther south outside previous distributional rangesA smaller number of Australia seabird species have maintainedstable populations or demonstrated no affects on breedingsuccess as a result of climatic variability A still smaller numberlike the Bridled Tern appear to be benefiting from increasedSSTs an effect that is probably associated with the southwardexpansion of tropical prey types Although constrained by anabsence of data on many species and regions our compilation ofexisting research on climatic effects on Australian seabirdsdemonstrates that the potential for further future detrimentaleffects from climate warming is high but that not all species orecosystems will be affected similarly

A majority of the studies presented here (Table 1) as well aselsewhere (eg Schreiber and Schreiber 1984 Bertram et al2005 Mills et al 2008 Ainley et al 2010) identified linksbetween climatic processes as associated with nutrient avail-ability in the food chain and seabirds Climatic variabilityinfluences ocean circulation which affects primary productivity(phytoplankton) secondary productivity (zooplankton) fishand finally predators (Brown et al 2010) Current modellingof projected primary productivity has suggested ecosystemsaround Australia will experience increases in primary produc-tivity and cascading benefits to the biomass of top predators asa result of plausible climate-change scenarios (Brown et al2010) However this lsquobottom-uprsquo approach may be too simplis-tic when predicting flow-on effects to seabirds (Hunt et al 2002Ainley et al 2007 Frank et al 2007 Cury et al 2008) Thecombined effects of climate change and overfishing may alterspatial occurrences of fish upon which a vast community


of seabirds feed despite high levels of primary productivity(Greacutemillet et al 2008) Similarly predatory fish (Worm andMyers 2003) and other top predators (Ainley et al 2006) mayexert an as-yet-unknown degree of lsquotop-downrsquo control It islikely that both top-down and bottom-up controlling processeswill occur simultaneously and the resultant dynamic betweenthese processes is presently unpredictable with similarly unpre-dictable consequences for seabird populations

There is no consistent indication of future changes in ENSOamplitude or frequency and the pragmatic and precautionaryapproach is to assume that ENSO events will continue as asource of significant interannual climate anomalies affectingthe marine environment (Holbrook et al 2009) However theinteraction of future ENSO events with SSTs higher than presentis expected to make effects associated with unusually warmwaters more severe For example more intense tropical cyclonesare expected to increase physical destruction of ecosystems suchas coral reefs and coastal margins during La Nintildea events(Holbrook et al 2009) Rainfall may become more extreme insome regions with more extended drought periods (associatedwith higher air temperatures) during El Nintildeo events Moreintense high-rainfall events are likely to increase freshwaterflow and sediment to coastal regions during La Nintildea eventsHigher sea levels which in addition to reducing land areas ofislands and cays are likely to increase effects of tropical andextra-tropical cyclones on coastal areas A reduction inthe overall intensity of the Leeuwin Current is expected andfurther increasing of SSTs around Australia is projected(Holbrook et al 2009 Lough 2009)

As a response to further rises in SSTs tropical seabirds maybe able to persist at more southerly latitudes than at present(Dunlop 2009) However the potential for seabirds to shiftbreeding locations will be highly dependent on future distribu-tions of suitable breeding habitats and prey distributions oropportunities to switch prey as well as overcoming any inertiaassociated with site fidelity (Congdon et al 2007 Dunlop 2009)Sea-level rise is likely to reduce existing breeding habitatparticularly for burrow- and surface-nesting species on low-lying islands at least in the short-term

This review highlights that seabirds are influenced bychanges in both the marine and terrestrial spheres and thecomplexity of the influences can make it difficult to anticipatethe likely effects of future climate change on individual speciesand regions Within the marine environment there appear to befew adaptation options that managers can implement to bufferthe potential effects of changing oceanographic conditionsalthough artificial structures may provide additional nestingsites Land-based management options to buffer anticipatedchanges in climate directly include habitat management toimprove microclimate or to reduce erosion However the great-est opportunities to increase the resilience of seabirds will mostlikely be through effective management of non-climatic threatssuch as predator control reducing anthropogenic competition forresources and protection of nests Further research and moni-toring both with Australia and overseas should help to bridgeexisting knowledge gaps including species and ecosystemvulnerabilities and thresholds of change and provide muchneeded information to enhance seabird management andconservation

Acknowledgements

The authors were brought together through their collaboration on a nationalmarine report card for Australia (Chambers et al 2009b) and as such wethank CSIRO and National Climate Change Adaptation Research Facility fortheir involvement Funding for parts of this research was provided by theQueensland Parks amp Wildlife Service The Marine and Tropical ScienceResearch Facility The Reef and Rainforest Research Centre A Great BarrierReef Marine Park Authority Science for Management Award anAIMSJCU PhD Scholarship and the Australian Research Council (ARCfunding LP 0562157) P Dann thanks the Phillip Island Nature Parks andDepartment of Sustainability and Environment (Victoria) for financialsupport We also acknowledge helpful comments on earlier versions byS Allen K Hulsman and the Emu reviewers

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Bertram D F Harfenist A and Smith B D (2005) Ocean climateand El Nintildeo impacts on survival of Cassinrsquos Auklets fromupwelling and downwelling domains of British Columbia CanadianJournal of Fisheries and Aquatic Sciences 62 2841ndash2853 doi101139f05-190

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Chambers L E (2004) The impact of climate on Little Penguin breedingsuccess BMRC Research Report Bureau of Meteorology ResearchCentre Melbourne

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Chambers L E Renwick L and Dann P (2009a) Climate fire and LittlePenguins In lsquoAustraliarsquos Biodiversity and Climate Changersquo (EdW Steffen) p 82 (CSIRO Publishing Melbourne)

Chambers L E Congdon B C Dunlop N Dann P and DevneyC (2009b) Seabirds and climate change In lsquoMarine Climate Change inAustralia Impacts and Adaptation Responses 2009 Report CardrsquoNCCARF Publication 0509 (Eds E S Poloczanska A J Hobday andA J Richardson) (National Climate Change Adaptation ResearchFacility) Available at httpwwwoceanclimatechangeorgaucontentimagesuploadsSeabirds_FINALvs2pdf [Verified 8 July 2011]

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Clout M N and Russell J C (2008) The invasion ecology of mammalsa global perspective Wildlife Research 35 180ndash184 doi101071WR07091

Congdon B C Krockenberger A K and Smithers B V (2005) Dual-foraging and co-ordinated provisioning in a tropical Procellariiformthe wedge-tailed shearwater Marine Ecology Progress Series 301293ndash301 doi103354meps301293

Congdon B C Erwin C A Peck D R Baker G B Double M C andOrsquoNeill P (2007) Vulnerability of seabirds on the Great Barrier Reef toclimate change In lsquoClimate Change and the Great Barrier Reefrsquo (EdsJ E Johnson and P A Marshall) pp 427ndash463 (Great Barrier ReefMarine Park Authority and Australian Greenhouse Office TownsvilleQLD)

Coulson J C and Coulson B A (2008) Measuring immigration andphilopatry in seabirds recruitment to Black-legged Kittiwake coloniesIbis 150 288ndash299 doi101111j1474-919X200700777x

Crawford R J M and Jahncke J (1999) Comparison of trends inabundance of guano-producing seabirds in Peru and southern AfricaSouth African Journal of Marine Science 21 145ndash156 doi102989025776199784126006

Croxall J P Trathan P N and Murphy E J (2002) Environmentalchange and Antarctic seabird populations Science 297 1510ndash1514doi101126science1071987

Cullen J M Chambers L E Coutin P and Dann P (2009) Predictingonset and success of breeding in Little Penguins Eudyptula minor fromocean temperatures Marine Ecology Progress Series 378 269ndash278doi103354meps07881

Cury P M Shin Y J Planque B Durant J M Fromentin J-MKramer-Schadt S Stenseth N C Travers M and Grimm V (2008)Ecosystem oceanography for global change in fisheries Trends inEcology amp Evolution 23 338ndash346 doi101016jtree200802005

Dann P (1991) Distribution population trends and factors influencing thepopulation size of Little Penguins Eudyptula minor on Phillip IslandVictoria Emu 91 263ndash272 doi101071MU9910263

Dann P and Chambers L (2009) Climate change and Little PenguinsWestern Port Greenhouse Alliance Melbourne Available at httpwwwclimatechangevicgovau__dataassetspdf_file0016106117Ecologi-calimpactsonPhillipIslandPenguinspdf [Verified 7 July 2001]

Dann P and Norman F I (2006) Population regulation in LittlePenguins Eudyptula minor the role of intraspecific competition fornesting sites and food during breeding Emu 106 289ndash296 doi101071MU06011

DECC (2007) Lord Howe Island Biodiversity Management Plan Depart-ment of Environment and Climate Change (NSW) Sydney

DEH (2004) National Recovery Plan for the Abbottrsquos Booby Papasulaabbotti Department of the Environment and Heritage Canberra

Devney C A and Congdon B C (2009) Testing the efficacy of aboundary fence on an important tropical seabird breeding colony andkey tourist destination Wildlife Research 36 353ndash360 doi101071WR08143

Devney C A Short M and Congdon B C (2009a) Sensitivity of tropicalseabirds to El Nintildeo precursors Ecology 90 1175ndash1183 doi10189008-06341

Devney C A Short M and Congdon B C (2009b) Cyclonic andanthropogenic influences on tern populations Wildlife Research 36368ndash378 doi101071WR08142

Devney C A Caley M J and Congdon B C (2010) Flexibility ofresponses by parent and offspring noddies to sea-surface temperatureanomalies PLoS ONE 5(7) e11891doi101371journalpone0011891


Doney S C Fabry V J Feely R A and Kleypas J A (2009) Oceanacidification the other CO2 problem Annual Review of Marine Science1 169ndash192 doi101146annurevmarine010908163834

Dunlop J N (2009) The population dynamics of tropical seabirds establish-ing frontier colonies on islands off south-western Australia MarineOrnithology 37 99ndash105

Dunlop J N Long P Stejskal I and Surman C (2002) Inter-annualvariations in breeding participation at fourWesternAustralian colonies ofthe Wedge-tailed Shearwater Puffinus pacificus Marine Ornithology 3013ndash18

Dupont S Dorey N and Thorndyke M (2010) What meta-analysis cantell us about vulnerability of marine biodiversity to ocean acidificationEstuarine Coastal and Shelf Science 89 182ndash185 doi101016jecss201006013

Durant J M Stenseth N C Anker-Nilssen T Harris M P ThompsonP M and Wanless S (2004) Marine birds and climate fluctuation inthe North Atlantic In lsquoMarine Ecosystems and Climate Variation TheNorth Atlantic ndash A Comparative Perspectiversquo (Eds N C StensethG Ottersen J W Hurrell and A Belgrano) pp 95ndash105 (OxfordUniversity Press Oxford UK)

Edwards M and Richardson A J (2004) Impact of climate change onmarine pelagic phenology and trophic mismatch Nature 430 881ndash884doi101038nature02808

Eriksson M O G (1985) Prey detectability for fish-eating birds in relationto fish density and water transparency Ornis Scandinavica 16 1ndash7doi1023073676567

Erwin RM (1980) Breeding habitat use by colonially nesting waterbirds intwo mid-Atlantic US regions under different regimes of human distur-bance Biological Conservation 18 39ndash51 doi1010160006-3207(80)90064-6

Erwin C A and Congdon B C (2007) Day-to-day variation in sea-surfacetemperature reduces Sooty Tern (Sterna fuscata) foraging success on theGreat Barrier Reef Australia Marine Ecology Progress Series 331255ndash266 doi103354meps331255

Fischer A and van der Wal R (2007) Invasive plant suppresses charis-matic seabird ndash the construction of attitudes towards biodiversity man-agement Biological Conservation 135 256ndash267 doi101016jbiocon200610026

Forcada J and Trathan P N (2009) Penguin responses to climate changein the Southern Ocean Global Change Biology 15 1618ndash1630doi101111j1365-2486200901909x

Fortescue M (1998) The marine and terrestrial ecology of a northernpopulation of the Little Penguin Eudyptula minor from Bowen IslandJervis Bay PhD Thesis University of Canberra Canberra

Frank K T Petrie B and Shackell N L (2007) The ups and downs oftrophic control in continental shelf ecosystems Trends in Ecology ampEvolution 22 236ndash242 doi101016jtree200703002

Frederiksen M Wanless S Harris M P Rothery P and Wilson L J(2004) The role of industrial fisheries and oceanographic change in thedecline of North Sea Black-legged Kittiwakes Journal of AppliedEcology 41 1129ndash1139 doi101111j0021-8901200400966x

Garnett S T and Crowley G M (2000) lsquoThe Action Plan for AustralianBirds 2000rsquo (Environment Australia Canberra) Available at httpwwwenvironmentgovaubiodiversitythreatenedpublicationsactionbirds2000indexhtml [Verified 7 July 2011]

Gaughan D Surman C Moran M Burbidge A andWooller R (2002)Feeding ecology of seabirds nesting at the Abrolhos Islands WesternAustralia Final report for FRDC Project 1998203 Department ofFisheries Perth

Gjerdrum C Valleacutee A M J Cassady St Clair C Bertram D F RyderJ L and Blackburn G S (2003) Tufted Puffin reproduction revealsocean climate variability Proceedings of the National Academy ofSciences of the United States of America 100 9377ndash9382 doi101073pnas1133383100

Greene C H and Pershing A J (2007) Climate drives sea change Science315 1084ndash1085 doi101126science1136495

Greacutemillet D and Boulinier T (2009) Spatial ecology and conservation ofseabirds facing global climate change a review Marine Ecology Prog-ress Series 391 121ndash137 doi103354meps08212

Greacutemillet D and Charmantier A (2010) Shifts in phenotypic plasticityconstrain the value of seabirds as ecological indicators of marineecosystems Ecological Applications 20 1498ndash1503 doi10189009-15861

Greacutemillet D Lewis S Drapeau L van der Lingen C D Huggett J ACoetzee J C Verheye H M Daunt F Wanless S and Ryan P G(2008) Spatial matchndashmismatch in the Benguela upwelling zone shouldwe expect chlorophyll and SST to predict marine predator distributionsJournal of Applied Ecology 45 610ndash621 doi101111j1365-2664200701447x

Grimes C B (2001) Fishery production and the Mississippi River dis-charge Fisheries (Bethesda Md) 26 17ndash26 doi1015771548-8446(2001)026lt0017FPATMRgt20CO2

Heatwole H OrsquoNeill P Jones M and Preker M (1996) Long-termpopulation trends of seabirds on the Swain Reefs Great Barrier ReefTechnical Report No 12 CRCReef Research Centre Townsville QLD

Henkel L A (2006) Effect of water clarity on the distribution of marinebirds in nearshore waters of Monterey Bay California Journal of FieldOrnithology 77 151ndash156 doi101111j1557-9263200600035x

Hill R and Dunn A (2004) National recovery plan for the ChristmasIsland Frigatebird (Fregata andrewsi) Commonwealth of AustraliaDepartment of the Environment and Heritage Canberra

Hoegh-Guldberg O Anthony K Berkelmans R Dove S Fabricus KLough J Marshall P van Oppen M J H Negri A and WilliesB (2007) Vulnerability of reef-building corals on the Great Barrier Reefto climate change In lsquoGreat Barrier Reef and Climate Change AVulnerability Assessmentrsquo (Eds J E Johnson and P A Marshall)pp 272ndash307 (Great Barrier Reef Marine Park Authority TownsvilleQLD)

Holbrook N J Davidson J Feng M Hobday A J Lough J MMcGregor S and Risbey S (2009) El NintildeondashSouthern Oscillation InlsquoMarine Climate Change in Australia Impacts andAdaptationResponses2009 Report Cardrsquo NCCARF Publication 0509 (Eds E S PoloczanskaA J Hobday and A J Richardson) (National Climate Change Adap-tation Research Facility) Available at httpwwwoceanclimatechangeorgaucontentimagesuploadsENSO-finalpdf [Verified 8 July 2011]

Hoskins A J Dann P Ropert-Coudert Y Kato A Chiaradia A CostaD P and Arnould J P Y (2008) Foraging behaviour and habitatselection at sea in Little Penguins Eudyptula minor during the chick-guard stage of breedingMarine Ecology Progress Series 366 293ndash303doi103354meps07507

House of Representatives (2009) Managing our coastal zone in a changingclimate the time to act is now House of Representatives StandingCommittee on Climate Change Water Environment and the Arts TheParliament of the Commonwealth of Australia Canberra

Hughes L (2000) Biological consequences of global warming is the signalalready apparentTrends in EcologyampEvolution 15 56ndash61 doi101016S0169-5347(99)01764-4

Hulsman K (1977) Breeding success and mortality of terns at One TreeIsland Great Barrier Reef Emu 77 49ndash60 doi101071MU9770049

Hunt G L and Schneider D C (1987) Scale-dependent processes in thephysical and biological environment of marine birds In lsquoSeabirdsFeeding Ecology and Role Marine Ecosystemsrsquo (Ed J P Croxall)pp 7ndash42 (Cambridge University Press Cambridge UK)

HuntGLJrStabenoPWaltersGSinclairEBrodeurRDNappJMand Bond N A (2002) Climate change and control of the southeasternBering Sea pelagic ecosystem Deep-sea Research Part II TopicalStudies in Oceanography 49 5821ndash5853 doi101016S0967-0645(02)00321-1


Hyrenbach K D Veit R R Weimerskirch H and Hunt G L Jr (2006)Seabird associations with mesoscale eddies the subtropical IndianOcean Marine Ecology Progress Series 324 271ndash279 doi103354meps324271

Hyrenbach K D Veit R R Weimerskirch H Metzl N and Hunt G LJr (2007) Community structure across a large-scale ocean productivitygradient marine bird assemblages of the southern Indian Ocean Deep-sea Research Part I Oceanographic Research Papers 54 1129ndash1145doi101016jdsr200705002

Jacobs S S Giulivi C F and Mele P A (2002) Freshening of the RossSea during the late 20th century Science 297 386ndash389 doi101126science1069574

Jaquemet S Le Corre M and Weimerskirch H (2004) Seabirdcommunity structure in a coastal tropical environment importance ofassociations with sub-surface predators and of fish aggregating devices(FADs) Marine Ecology Progress Series 268 281ndash292 doi103354meps268281

Jenouvrier S Barbraud C and Weimerskirch H (2003) Effects ofclimate variability on the temporal population dynamics of SouthernFulmars Journal of Animal Ecology 72 576ndash587 doi101046j1365-2656200300727x

King B R (1996) The status of seabirds in Queensland In lsquoThe Status ofAustraliarsquos Seabirds Proceedings of the National Seabird WorkshopCanberra 1ndash2 November 1993rsquo (Eds G J B Ross K Weaver andJ C Greig) pp 211ndash233 (Biodiversity Group Environment AustraliaCanberra)

King B R Hicks J T and Cornelius J (1992) Population changesbreeding cycles and breeding success over six years in a seabird colonyat Michaelmas Cay Queensland Emu 92 1ndash10 doi101071MU9920001

Kitaysky A S and Golubova E G (2000) Climate change causescontrasting trends in reproductive performance of planktivorous andpiscivorous alcids Journal of Animal Ecology 69 248ndash262 doi101046j1365-2656200000392x

Langham N P and Hulsman K (1986) The breeding biology ofthe Crested Tern Sterna bergii Emu 86 23ndash32 doi101071MU9860023

Lewison R L Crowder L B Read A J and Freeman S A (2004)Understanding impacts of fisheries bycatch on marine megafaunaTrends in Ecology amp Evolution 19 598ndash604 doi101016jtree200409004

Lough J M (2009) Temperature In lsquoMarine Climate Change in AustraliaImpacts and Adaptation Responses 2009 Report Cardrsquo NCCARF Pub-lication 0509 (Eds E S Poloczanska A J Hobday andA J Richardson) (National Climate Change Adaptation ResearchFacility) Available at httpwwwoceanclimatechangeorgaucontentimagesuploadsTemperaturepdf [Verified 8 July 2011]

McPhaden M J and Yu X (1999) Genesis and evolution of the1997ndash1998 El Nintildeo Science 283 950ndash954 doi101126science2835404950

Mills J A Yarrall J W Bradford-Grieve J M Uddstrom M JRenwick J A and Merila J (2008) The impact of climatefluctuation on food availability and reproductive performance of theplanktivorous Red-billed Gull Larus novaehollandiae scopulinus Jour-nal of Animal Ecology 77 1129ndash1142 doi101111j1365-2656200801383x

Moe B Brunvoll S Mork D Brobakk T E and Bech C (2004)Developmental plasticity of physiology and morphology in diet-restrict-ed European Shag nestlings (Phalacrocorax aristotelis) Journal ofExperimental Biology 207 4067ndash4076 doi101242jeb01226

Nevitt G A (2008) Sensory ecology on the high seas the odor world of theProcellariiform seabirds Journal of Experimental Biology 2111706ndash1713 doi101242jeb015412

Norman F I (1970) The effects of sheep on the breeding success and habitatof the Short-tailed Shearwater Puffinus tenuirostris (Temminck) Aus-tralian Journal of Zoology 18 215ndash229 doi101071ZO9700215

Norman F I (1974) Notes on the breeding of the Pied Cormorant nearWerribee Victoria in 1971 1972 and 1973 Emu 74 223ndash227doi101071MU974223

Norman I Dann P and Menkhorst P (1996) The status of seabirds inVictoria In lsquoThe Status of Australiarsquos Seabirds Proceedings of theNational Seabird Workshop 1ndash2 November 1993 Canberrarsquo (EdsG J B Ross K Weaver and J C Greig) pp 185ndash200 (BiodiversityGroup Environment Australia Canberra)

Nussey D H Wilson A J and Brommer J E (2007) The evolutionaryecology of individual phenotypic plasticity in wild populations Journalof Evolutionary Biology 20 831ndash844 doi101111j1420-9101200701300x

OrsquoBrien D P (1988) Surface schooling behaviour of the coastal krillNyctiphanes australis (CrustaceaEuphausiacea) off Tasmania Austra-lia Marine Ecology Progress Series 42 219ndash233 doi103354meps042219

Oedekoven C S Ainley D G and Spear L B (2001) Variable responsesof seabirds to change in marine climate California Current 1985ndash1994Marine Ecology Progress Series 212 265ndash281 doi103354meps212265

Olsen P (2007) The State ofAustraliarsquosBirds 2007Wingspan14(4 Suppl)Orr J C Fabry V J Aumont O Bopp L Doney S C Feely R A

Gnanadesikan A Gruber N Ishida A Joos F et al (2005)Anthropogenic ocean acidification over the twenty-first century and itsimpact on calcifying organisms Nature 437 681ndash686 doi101038nature04095

Peck D R and Congdon B C (2005) Colony-specific foraging behaviourand co-ordinated divergence of chick development in the Wedge-tailedShearwater Puffinus pacificus Marine Ecology Progress Series 299289ndash296 doi103354meps299289

Peck D R Smithers B V Krockenberger A K and Congdon B C(2004) Sea-surface temperature constrains Wedge-tailed Shearwaterforaging success within breeding seasons Marine Ecology ProgressSeries 281 259ndash266 doi103354meps281259

Pendlebury S F and Barnes-Keoghan I P (2007) Climate and climatechange in the sub-AntarcticPapers and Proceedings of the Royal Societyof Tasmania 141 67ndash82

Poloczanska E S Babcock R C Butler A Hobday A J Hoegh-Guldberg O Kunz T J Matear R Milton D A Okey T A andRichardson A J (2007) Climate change and Australian marine life InlsquoOceanography and Marine Biology An Annual Reviewrsquo Vol 45 (EdsR N Gibson J A Atkinson J D M Gordon) pp 407ndash478 (CRCPress Boca Raton FL)

Post E Brodie J Hebblewhite M Anders A D Maier J A K andWilmers C C (2009) Global population dynamics and hot spots ofresponse to climate change Bioscience 59 489ndash497 doi101525bio20095967

Quillfeldt P Strange I J and Masello J F (2007) Sea surface tempera-tures and behavioural buffering capacity in Thin-billed Prions Pachyptilabelcheri breeding success provisioning and chick begging Journal ofAvian Biology 38 298ndash308

Ramos J A Maul A M Ayrton V Bullock I Hunter J Bowler JCastle G Mileto R and Pacheco C (2002) Influence of local andlarge-scale weather events and timing of breeding on tropical RoseateTern reproductive parameters Marine Ecology Progress Series 243271ndash279 doi103354meps243271

Ramos J A Maul A M Bowler J Wood L Threadgold R JohnsonS Birch D and Walker S (2006) Annual variation in laying date andbreeding success of Brown Noddies on Aride Island Seychelles Emu106 81ndash86 doi101071MU05023


Raymond B Shaffer S A Sokolov S Woehler E J Costa D PEinoder L Hindell M Hosie G Pinkerton M Sagar P M ScottD Smith A Thompson D R Vertigan C and Weimerskirch H(2010) Shearwater foraging in the Southern Ocean the roles of preyavailability and winds PLoS ONE 5(6) e10960doi101371journalpone0010960

Reacuteale D McAdam A G Boutin S and Berteaux D (2003) Genetic andplastic responses of a northern mammal to climate change Proceedingsof the Royal Society of London Series B Biological Sciences 270591ndash596 doi101098rspb20022224

Reed T E Warzybok P Wilson A J Bradley R W Wanless S andSydeman W J (2009) Timing is everything flexible phenology andshifting selection in a colonial seabird Journal of Animal Ecology 78376ndash387 doi101111j1365-2656200801503x

Regehr H M and Montevecchi W A (1997) Interactive effects of foodshortage and predation on breeding failure of Black-legged Kittiwakesindirect effects of fisheries activities and implications for indicatorspecies Marine Ecology Progress Series 155 249ndash260 doi103354meps155249

Reville B J Tranter J D and Yorkston H D (1990) Conservation of theendangered seabird Abbottrsquos Booby on Christmas Island 1983ndash1989ANPWS Occasional Paper 20 Australian National Parks and WildlifeService Canberra

RichardsonA Poloczanska E S andMilton D (2006) Impacts of climatechange on seabirds In lsquoImpacts of Climate Change on Australian MarineLifersquo Report to the Australian Greenhouse Office (Eds A J HobdayT A Okey E S Poloczanska T J Kunz and A J Richardson)pp 110ndash113(Australian Greenhouse Office Canberra)

Rodgers J A and Smith H T (1995) Set-back distances to protect nestingbird colonies from human disturbance in Florida Conservation Biology9 89ndash99 doi101046j1523-1739199509010089x

Rolland V Weimerskirch H and Barbraud C (2010) Relative influenceof fisheries and climate on the demography of four albatross speciesGlobal Change Biology 16 1910ndash1922 doi101111j1365-2486200902070x

Root T L Price J T Hall K R Schneider S H Rosenzweig C andPounds J A (2003) Fingerprints of global warming on wild animalsand plants Nature 421 57ndash60 doi101038nature01333

Ropert-Coudert Y Kato A and Chiaradia A (2009) The impact ofsmall-scale environmental perturbations on local marine food resourcesa case study of a predator the Little Penguin Proceedings of the RoyalSociety of London Series B Biological Sciences 276 4105ndash4109doi101098rspb20091399

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Ross G J B Weaver K and Greig J C (Eds) (1996) lsquoThe Status ofAustraliarsquos Seabirds Proceedings of the National Seabird WorkshopCanberra 1ndash2 November 1993rsquo (Biodiversity Group EnvironmentAustralia Canberra)

Roughan M and Middleton J H (2002) A comparison of observedupwelling mechanisms off the east coast of Australia Continental ShelfResearch 22 2551ndash2572 doi101016S0278-4343(02)00101-2

Sandvik H and Erikstad K E (2008) Seabird life histories and climaticfluctuations a phylogenetic-comparative time series analysis ofNorth Atlantic seabirdsEcography 31 73ndash83 doi101111j20070906-759005090x

Sandvik H Erikstad K E Barrett R T and Yoccoz N G (2005) Theeffect of climate on adult survival in five species of North Atlanticseabirds Journal of Animal Ecology 74 817ndash831 doi101111j1365-2656200500981x

Sandvik H Coulson T and Saeligther B-E (2008) A latitudinal gradient inclimate effects on seabird demography results from interspecific anal-yses Global Change Biology 14 703ndash713 doi101111j1365-2486200701533x

Santojanni A Arneri E Bernardini V Cingolani N Di Marco M andRusso A (2006) Effects of environmental variables on recruitment ofanchovy in the Adriatic Sea Climate Research 31 181ndash193doi103354cr031181

Schreiber R W and Schreiber E A (1984) Central Pacific seabirds andthe El Nintildeo Southern Oscillation 1982 to 1983 perspectives Science225 713ndash716 doi101126science2254663713

Sharples C (2006) lsquoIndicative Mapping of Tasmanian Coastal Vulnera-bility to Climate Change and Sea-Level Rise Explanatory Reportrsquo2nd edn (Department of Primary Industries and Water Hobart)

Sidhu L (2007) Analysis of recovery-recapture data for Little PenguinsPhD Thesis University of New South Wales at the Australian DefenceForce Academy Canberra

Smith A M (2009) Bryozoans as southern sentinels of ocean acidificationa major role for a minor phylum Marine and Freshwater Research 60475ndash482 doi101071MF08321

Smith R C Domack E Emslie S FraserW R Ainley D G Baker KKennett J Leventer A Mosley-Thompson E Stammerjohn S andVernet M (1999) Marine ecosystem sensitivity to historical climatechange Antarctic Peninsula Bioscience 49 393ndash404 doi1023071313632

Smithers B V Peck D R Krockenberger A K and Congdon B C(2003) Elevated sea-surface temperature reduced provisioning andreproductive failure of Wedge-tailed Shearwaters (Puffinus pacificus) inthe southern Great Barrier Reef Marine and Freshwater Research 54973ndash977 doi101071MF02137

Stahel C and Gales R (1987) lsquoLittle Penguin Fairy Penguins inAustraliarsquo (New South Wales University Press Sydney)

Steffen W Burbridge A A Hughes L Kitching R Lindenmayer DMusgraveW Stafford SmithM andWerner P A (2009) lsquoAustraliarsquosBiodiversity and Climate Changersquo (CSIRO Publishing Melbourne)

Stenseth N C Mysterud A Ottersen G Hurrell J W Chan K-S andLima M (2002) Ecological effects of climate fluctuations Science297 1292ndash1296 doi101126science1071281

Surman C A and Nicholson L (2009) The good the bad and the uglyENSO-driven oceanographic variability and its influence on seabird dietand reproductive performance at the Houtman Abrolhos eastern IndianOcean Marine Ornithology 37 129ndash138

Surman C A and Wooller R D (1995) The breeding biology of theLesser Noddy on Pelsaert Island Western Australia Emu 95 47ndash53doi101071MU9950047

Suryan RM Saba V S Wallace B P Hatch S A Frederiksen M andWanless S (2009) Environmental forcing on life history strategiesevidence for multi-trophic level responses at ocean basin scalesProgress in Oceanography 81 214ndash222 doi101016jpocean200904012

Sydeman W J and Bograd S J (2009) Marine ecosystems climate andphenology introductionMarine Ecology Progress Series 393 185ndash188doi103354meps08382

Taylor A (2007)Winter breeding in a temperate cormorant the Black-facedCormorant Phalacrocorax fuscescens BSc(Hons) Thesis Deakin Uni-versity Burwood VIC

Tierno de Figueroa J M T Loacutepez-Rodriacuteguez M J Lorenz A Graf WSchmidt-Kloiber A and Hering D (2010) Vulnerable taxa of Euro-pean Plecoptera (Insecta) in the context of climate change Biodiversityand Conservation 19 1269ndash1277 doi101007s10531-009-9753-9

Trathan P N Forcada J and Murphy E J (2007) Environmental forcingand Southern Ocean marine predator populations effects of climatechange and variability Philosophical Transactions of the Royal Societyof London Series B Biological Sciences 362 2351ndash2365 doi101098rstb20061953


Turner M and Batianoff G N (2007) Vulnerability of island flora andfauna in the Great Barrier Reef to climate change In lsquoClimate Changeand the Great Barrier Reefrsquo (Eds J E Johnson and P A Marshall)pp 621ndash666 (Great Barrier Reef Marine Park Authority and AustralianGreenhouse Office Townsville QLD)

van Tets G F and Fullagar P J (1984) Status of seabirds breeding inAustralia In lsquoStatus and Conservation of the Worldrsquos Seabirdsrsquo Inter-national Council for Bird Preservation Technical Publication 2 (EdsJ P Croxall P G H Evans and R W Shreiber) pp 559ndash571(International Council for Bird Preservation Cambridge UK)

Veit R RMcGowan J A Ainley D GWahls T R and Pyle P (1997)Apex marine predator declines ninety percent in association withchanging ocean climate Global Change Biology 3 23ndash28 doi101046j1365-24861997d01-130x

Velarde E Ezcurra E Cisneros-Mata M A and Lavin M F (2004)Seabird ecology El Nintildeo anomalies and prediction of sardine fisheriesin the Gulf of California Ecological Applications 14 607ndash615doi10189002-5320

Voigts D K (1999) Observations of a colony of roof-nesting Least Terns1988ndash1997 Florida Field Naturalist 27 103ndash108

Votier S C Hatchwell B J Beckerman A McCleery R H HunterF M Pellatt J Trinder M and Birkhead T R (2005) Oil pollutionand climate have wide-scale impacts on seabird demographics EcologyLetters 8 1157ndash1164 doi101111j1461-0248200500818x

Walker T A (1991) Pisonia islands of the Great Barrier Reef I Thedistribution abundance and dispersal by seabirds of Pisonia grandisAtoll Research Bulletin 350 1ndash23

Walther G R Post E Convey P Menzel A Parmesan C BeebeeT J C Fromentin J-M Hoegh-Guldberg O and Bairlein F (2002)Ecological responses to recent climate change Nature 416 389ndash395doi101038416389a

WeerheimM S KlompN I Brunsting AMH andKomdeur J (2003)Population size breeding habitat and nest site distribution of LittlePenguins (Eudyptula minor) on Montague Island New South WalesWildlife Research 30 151ndash157 doi101071WR02115

Weimerskirch H Inchausti P Guinet C and Barbraud C (2003) Trendsin bird and seal populations as indicators of a system shift in theSouthern Ocean Antarctic Science 15 249ndash256 doi101017S0954102003001202

Weimerskirch H Le Corre M Jaquemet S and Marsac F (2005)Foraging strategy of a tropical seabird the Red-footed Booby in adynamic marine environment Marine Ecology Progress Series 288251ndash261 doi103354meps288251

Woehler E J (2006) Status and conservation of the seabirds of HeardIsland and the McDonald Islands In lsquoHeard Island Southern OceanSentinelrsquo (Eds K Green and E J Woehler) pp 128ndash165 (Surrey Beattyand Sons Sydney)

Woehler E J Auman H J and RiddleM J (2002) Long-term populationincrease of Black-browed Albatrosses Thalassarche melanophrys atHeard Island 19471948 ndash 20002001 Polar Biology 25 921ndash927

Woehler E J Raymond B and Watts D J (2006) Convergence ordivergence where do Short-tailed Shearwaters forage in the SouthernOcean Marine Ecology Progress Series 324 261ndash270 doi103354meps324261

Worm B and Myers R A (2003) Meta-analysis of codndashshrimp interac-tions reveals top-down control in oceanic food-web Ecology 84162ndash173 doi1018900012-9658(2003)084[0162MAOCSI]20CO2

Manuscript received 10 May 2010 accepted 19 January 2011


httpwwwpublishcsiroaujournalsemu

north-western Atlantic Ocean reduced breeding success hasbeen associated with lower SSTs (Regehr and Montevecchi1997 Sandvik et al 2008)

Whether seabirds can respond to further predicted changes inenvironmental variability remains largely unknown (Greacutemilletand Charmantier 2010) Adjustments to characteristics such asbehaviour diet morphology geographical distribution or phe-nology to suit changing environmental conditions can fostergreater lifetime reproductive success (Nussey et al 2007 Reedet al 2009) and population viability Organisms with suchplasticity will generally be better able to cope with environmen-tal variation and extremes (Reacuteale et al 2003 Moe et al 2004Chiaradia and Nisbet 2006)

Most studies into the potential effects of current and futureclimate variability on seabird biology have focused on high-latitude species in the northern Pacific Ocean (Veit et al 1997Ainley and Divoky 2001 Bertram et al 2009) northern AtlanticOcean (Durant et al 2004 Sandvik and Erikstad 2008 Sandviket al 2008) and the Southern Ocean (Smith et al 1999 Croxallet al 2002 Jenouvrier et al 2003 Barbraud and Weimerskirch2006 Forcada and Trathan 2009) Considerably less is knownabout species living in the south-western Pacific or the waterssurrounding Australia (but see Mills et al 2008) As a conse-quence there is little broad-scale information about the degreeto which particular species populations or ecosystems arevulnerable to climatic variation and whether plasticity in life-history characteristics or adaptation is likely to moderate theseeffects

Australia and its external territories have a diverse seabirdfauna of 110 species in 12 families (van Tets and Fullagar 1984Ross et al 1995) Most (69) also breed in the Australianregion with the rest being either regular or occasional visitorsduring the non-breeding season (Ross et al 1995) Effectivelong-term conservation of this diverse fauna in the face ofpredicted climate change requires a detailed understanding ofthe influence of large-scale and local climatic phenomena onreproductive and other life-history parameters across a range ofseabirds including representatives from different foragingguilds

This review aims to collate and summarise information onthe relationships between population demographic and beha-vioural characteristics of Australian seabirds and key large-scaledrivers of climate in the Australasian region such as ENSO andassociated oceanographic changes sea-level rise land tempera-tures and extreme events including cyclones floods and fireThis information is then used to identify consistent long-term demographic trends potentially linked to specific climaticphenomenon establish the nature and likely magnitude ofeffects on different foraging guild and species assess theirpotential to cope with such effects and identify existing knowl-edge gaps

Observed and projected changes

Effect of changes in ENSO ocean temperaturecurrents and stratification

ENSO is a major contributor to Australiarsquos climate and affectsAustraliarsquos marine waters to differing degrees in different coastalregions ENSO has a strong and very significant effect on the

intensity of the southward flowing Leeuwin Current and watersof Australiarsquos western coast (Holbrook et al 2009) ENSO isobserved as a weaker signal in the southward flowing EastAustralian Current along Australiarsquos eastern coast El Nintildeoevents are associated with a range of climatic anomalies inAustralian waters including increased SSTs (Holbrook et al2009) SSTs in the waters surrounding Australia have warmedsignificantly since the early 20th century (+07C Lough 2009)and 6 of the 10 warmest years have occurred in the most recent10 years (based on data back to 1910) By the 2030s SSTsaround Australia are projected to be ~1C warmer (relative to1980ndash99) with slightly less warming to the south of thecontinent By the 2070s SSTs are projected to be between15ndash30C warmer with slightly less warming to the south ofthe continent and greatest warming east and north-east ofTasmania (Lough 2009)

At the Houtman Abrolhos Western Australia (Fig 1) in-creased breeding deferral and reduced success in Wedge-tailedShearwaters (Ardenna pacifica) and tropical pelagic-foragingterns (eg Sooty Tern Onychoprion fuscata) tends to occurduring stronger ENSO events (Dunlop et al 2002 Surman andNicholson 2009) probably owing to changes in marine produc-tivity driven by associated oceanographic changes (ie currentsSST) (Dunlop et al 2002) During El Nintildeo events the ternspecies also tended to breed later (Surman and Nicholson 2009)presumably as a result of ENSO-linked weakening of theLeeuwin Current and a zonal shift in productivity In contrasta combination of both large-scale and local climatic conditionsappears to influence the breeding dynamics of Wedge-tailedShearwaters in this region with the number of burrows exca-vated being related to the cumulative effect of oceanic conditions(eg Southern Oscillation Index (SOI)) from previous seasonsand the number of eggs laid being related to local weather andpredation (Dunlop et al 2002) Importantly these negativeeffects have only been observed for pelagic and offshore-for-aging species with no similar influences detected on the inshoreforaging Crested Terns (Thalasseus bergii) (Gaughan et al2002) This is mostly likely because they have more flexibleforaging behaviours (Surman and Wooller 1995 Blaber et al1998) Breeding success and breeding effort in Red-billedGulls (Chroicocephalus novaehollandiae scopulinus) inNew Zealand were strongly correlated with ENSO events andavailability of prey species (Mills et al 2008) The results for thisNew Zealand subspecies of the Silver Gull (C novaehollandiaenovaehollandiae) of Australia may provide insights intoclimatendashprey relationships for Silver Gulls and similar speciesin Australia

ENSO events have also been associated with WesternAustralian tropical seabirds (including Wedge-tailed Shear-waters Red-tailed Tropicbirds (Phaethon rubricauda) CrestedRoseate (Sterna dougallii) Sooty and Bridled Terns (Onycho-prion anaethetus) and Common Noddies (Anous stolidus))prospecting and nesting beyond their accepted breeding distri-butions on the western coast This suggests that in philopatricspecies ENSO-related marine productivity failures maydrive the dispersal of pre-breeders to foraging areas awayfrom natal colonies during the breeding season (Dunlop2009) If so then predicted background rises in sea temperature(Lough 2009) may then enable tropical seabird prey and seabird








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10degS

20degS

30degS

40degS

10degS

20degS

30degS

40degS












































































































































Research priorities








Conclusions








Acknowledgements


References















































































































































































































































































































Research priorities








Conclusions








Acknowledgements


References












































































































































































Acknowledgements


References








































































































































































observed and predicted effects of climate on australian seabirds

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